Where do you know what you know? The representation of semantic knowledge in the human brain

Nature Reviews Neuroscience

Volumn 8, Issue 12, 2007, Pages 976-987

  Patterson, Karalyn ^a   Nestor, Peter J ^b   Rogers, Timothy T ^c  

^a MRC COGNITION AND BRAIN SCIENCES UNIT   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALZHEIMER DISEASE; BRAIN; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HERPES SIMPLEX ENCEPHALITIS; HUMAN; KNOWLEDGE; MATHEMATICAL MODEL; NEUROIMAGING; PRIORITY JOURNAL; REVIEW; SEMANTIC MEMORY; TEMPORAL LOBE;

BRAIN; BRAIN MAPPING; CONCEPT FORMATION; HUMANS; NERVE NET; SEMANTICS;

OVIS ARIES;

EID: 36348949178     PISSN: 1471003X     EISSN: 14710048     Source Type: Journal    
DOI: 10.1038/nrn2277     Document Type: Review

References (114)

1. Tulving, E. in Organisation of Memory (eds Tulving, E. & Donaldson, W.) 381-403 (Academic, New York, 1972).
2. Fodor, J. A. The Modularity of Mind (MIT Press, Cambridge, Massachusetts, USA, 1983).
3. Thompson-Schill, S. L. Neuroimaging studies of semantic memory: inferring "how" from "where". Neuropsychologia 41, 280-292 (2003). This review of neuropsychological and functional imaging studies offers a succinct overview of the modality-specific components of the cortical semantic network and addresses the role of prefrontal regions in control or selection of semantic information.
4. Allport, D. A. in Current Perspectives in Dysphasia (eds Newman, S. K. & Epstein, R.) 32-60 (Churchill Livingston, Edinburgh, 1985).
5. Martin, A. The representation of object concepts in the brain. Annu. Rev. Psychol. 58, 25-45 (2007). This is an elegant review of evidence for a distributed network of semantic features linked to the sensory and motor systems that analyse such features as input. It also argues for categorical organization of semantic memory.
6. Saffran, E. M. & Schwartz, M. F. in Attention and Performance XV (eds Umilta, C. & Moscovitch, M.) 507-535 (Lawrence Erlbaum Associates Inc., Hillsdale, 1994).
7. Riddoch, M. J., Humphreys, G. W., Coltheart, M. & Funnell, E. Semantic systems or system? Neuropsychological evidence re-examined. Cogn. Neuropsychol. 5, 3-25 (1988).
8. Caramazza, A., Hillis, A. E., Rapp, B. C. & Romani, C. The multiple semantic hypothesis: multiple confusions? Cogn. Neuropsychol. 7, 161-189 (1990).
9. Damasio, A. R. The brain binds entities and events by multiregional activation from convergence zones. Neural Comput. 1, 123-132 (1989).
10. Damasio, A. R. & Damasio, H. in Large-Scale Neuronal Theories of the Brain (ed. Koch, C.) 61-74 (MIT Press, Cambridge, Massachusetts, USA, 1994).
11. Damasio, H., Grabowski, T. J., Tranel, D., Hichwa, R. D. & Damasio, A. R. A neural basis for lexical retrieval. Nature 380, 499-505 (1996). This landmark paper combined lesion analysis in a large group of patients and PET imaging in normal individuals to identify brain regions crucial to retrieval of names for entities in different semantic categories (famous people, animals and tools).
12. Tranel, D., Damasio, H. & Damasio, A. R. A neural basis for the retrieval of conceptual knowledge. Neuropsychologia 35, 1319-11327 (1997).
13. Damasio, H., Tranel, D., Grabowski, T., Adolphs, R. & Damasio, A. R. Neural systems behind word and concept retrieval. Cognition 92, 179-229 (2004).
14. Beauchamp, M. S., Argall, B. D., Bodurka, J., Duyn, J. H. & Martin, A. Unravelling multisensory integration: patchy organization within human STS multisensory cortex. Nature Neurosci. 7, 1190-1192 (2004).
15. Snowden, J. S., Neary, D. & Mann, D. M. A. Fronto-Temporal Lobar Degeneration: Fronto-Temporal Dementia, Progressive Aphasia, Semantic Dementia (Churchill Livingstone, New York, 1996).
16. Davies, R. R. et al. The pathological basis of semantic dementia. Brain 128, 1962-1963 (2005).
17. Warrington, E. K. The selective impairment of semantic memory. Q. J. Exp. Psychol. 27, 635-657 (1975). This article represents one of the first, and still one of the very best and most creative, neuropsychological investigations of semantic dementia.
18. Schwartz, M. F., Martin, O. S. M. & Saffran, E. M. Dissociations of language function in dementia: a case study. Brain Lang. 7, 277-306 (1979).
19. Snowden, J. S., Goulding, P. J. & Neary, D. Semantic dementia: a form of circumscribed cerebral atrophy. Behav. Neurol. 2, 111-138 (1989).
20. Delacourte, A. et al. The biochemical pathway of neurofibrillary degeneration in aging and Alzheimer's disease. Neurology 52, 1158-1165 (1999).
21. Nestor, P. J., Fryer, T. D., Smielewski, P. & Hodges, J. R. Limbic hypometabolism in Alzheimer's disease and mild cognitive impairment. Ann. Neurol. 54, 343-351 (2003).
22. Giffard, B. et al. The nature of semantic memory deficits in Alzheimer's disease. Brain 124, 1522-1532 (2001).
23. Grossman, M. et al. Neural basis for semantic memory difficulty in Alzheimer's disease: an fMRI study. Brain 126, 292-311 (2003).
24. Galton, C. J., Patterson, K., Xuereb, J. H. & Hodges, J. R. Atypical and typical presentations of Alzheimer's disease: a clinical, neuropsychological, neuroimaging and pathological study of 13 cases. Brain 123, 484-498 (2000).
25. Lambon Ralph, M. A., Lowe, C. & Rogers, T. T. Neural basis of category-specific deficits for living things: evidence from semantic dementia, HSVE and a neural network model. Brain 130, 1127-1137 (2007).
26. Noppeney, U. et al. Temporal lobe lesions and semantic impairment: a comparison of herpes simplex virus encephalitis and semantic dementia. Brain 130, 1138-1147 (2007).
27. Caramazza, A. & Shelton, J. R. Domain specific knowledge systems in the brain: the animate-inanimate distinction. J. Cogn. Neurosci. 10, 1-34 (1998).
28. Farah, M. J. & McClelland, J. L. A computational model of semantic memory impairment: modality specificity and emergent category specificity. J. Exp. Psychol. Gen. 120, 339-357 (1991).
29. Warrington, E. K. & Shallice, T. Category-specific semantic impairment. Brain 107, 829-854 (1984).
30. Shallice, T. From Neuropsychology to Mental Structure (Cambridge Univ. Press, Cambridge, UK 1998).
31. Jefferies, E. & Lambon Ralph, M. A. Semantic impairment in stroke aphasia versus semantic dementia: a case-series comparison. Brain 129, 2132-2147 (2006).
32. Jefferies, E., Patterson, K. & Lambon Ralph, M. A. Deficits of knowledge vs. executive control in semantic cognition: insights from cued naming. Neuropsychologia 18 Sep 2004 (doi:10.1016/j.neuropsychologia. 2007.09.007).
33. Graham K., Patterson, K. & Hodges, J. R. Progressive pure anomia: insufficient activation of phonology by meaning. Neurocase 1, 25-38 (1995).
34. Berthier, M. Transcortical Aphasias (Psychology, Hove East Sussex, 1999).
35. Badre, D., Poldrack, R., Paré-Blagoev E., Insler R. & Wagner, A. Dissociable controlled retrieval and generalized selection mechanisms in ventrolateral prefrontal cortex. Neuron 47, 907-918 (2005).
36. Gold, B. T. et al. Dissociation of automatic and strategic lexical-semantics: functional magnetic resonance imaging evidence for differing roles of multiple frontotemporal regions. J. Neurosci. 26, 6523-6532 (2006).
37. Diehl, B. et al. Cerebral metabolic patterns at early stages of frontotemporal dementia and semantic dementia. A PET study. Neurobiol. Aging 25, 1051-1056 (2004).
38. Desgranges, B. et al. Anatomical and functional alterations in semantic dementia: a voxel-based MRI and PET study. Neurobiol. Aging 28,1904-1913.
39. Nestor, P. J., Fryer T. D. & Hodges J. R. Declarative memory impairments in Alzheimer's disease and semantic dementia. Neuroimage 30, 1010-1020 (2006). This study highlighted that the lesions (defined by FDG-PET metabolism) associated with the semantic deficit in semantic dementia are restricted to the anterior temporal lobes, whereas posterior temporal hypometabolism was evident in an Alzheimer group with absent or very mild semantic deficits.
40. Chan, D. et al. Patterns of temporal lobe atrophy in semantic dementia and Alzheimer's disease. Ann. Neurol. 49, 433-442 (2001).
41. Davies, R. R., Graham, K. S., Xuereb, J. H., Williams, G. B. & Hodges, J. R. The human perirhinal cortex and semantic memory. Eur. J. Neurosci. 20, 2441-2446 (2004).
42. Mummery, C. J. et al. A voxel-based morphometry study of semantic dementia: relationship between temporal lobe atrophy and semantic memory. Ann. Neurol. 47, 36-45 (2000).
43. Seeley, W. W. et al. The natural history of temporal variant frontotemporal dementia. Neurology 64, 1384-1390 (2005).
44. Chao, L. L., Haxby, J. V. & Martin, A. Attribute-based neural substrates in temporal cortex for perceiving and knowing about objects. Nature Neurosci. 2, 913-919 (1999).
45. Goldberg, R. F., Perfetti, C. A. & Schneider, W. Perceptual knowledge retrieval activates sensory brain regions. J. Neurosci. 26, 4917-4921 (2006).
46. Hauk, O., Johnsrude, I. & Pulvermuller, F. Somatotopic representation of action words in human motor and premotor cortex. Neuron 41, 301-307 (2004).
47. James, T. W. & Gauthier, I. Auditory and action semantic features activate sensory-specific perceptual brain regions. Curr. Biol. 13, 1792-1796 (2003).
48. Kellenbach, M. L., Brett, M. & Patterson, K. Large, colourful or noisy? Attribute- and modality-specific activations during retrieval of perceptual attribute knowledge. Cogn. Affect. Behav. Neurosci. 1, 207-221 (2001).
49. Kellenbach, M. L., Brett, M. & Patterson, K. Actions speak louder than functions: the importance of manipulability and action in tool representations. J. Cogn. Neurosci. 15, 20-46.
50. Joseph, J. E. Functional neuroimaging studies of category specificity in object recognition: a critical review and meta-analysis. Cogn. Affect. Behav. Neurosci. 1, 119-136.
51. Moore, C. J. & Price, C. J. Three distinct ventral occipitotemporal regions for reading and object naming. Neuroimage 10, 181-192 (1999).
52. 150-PET was largely absent with fMRI - a consequence of MRI susceptibility artefact.
53. Mummery, C. J., Patterson, K., Hodges, J. R. & Wise, R. J. S. Generating 'tiger' as an animal name or a word beginning with T: differences in brain activation. Proc. Biol. Sci. 263, 989-995 (1996).
54. Price, C. J., Devlin, J. T., Moore, C. J., Morton, C. & Laird, A. R. Meta-analyses of object naming: effect of baseline. Hum. Brain Mapp. 25, 70-82 (2005).
55. Rogers, T. T. et al. Anterior temporal cortex and semantic memory: reconciling findings from neuropsychology and functional imaging. Cogn. Affect. Behav. Neurosci. 6, 201-213 (2006).
56. Bright, P., Moss, H. & Tyler, L. K. Unitary vs multiple semantics: PET studies of word and picture processing. Brain Lang. 89, 417-432 (2004). This publication is significant because its conjunction analysis of four PET studies, using different kinds of semantic tasks and stimuli, revealed common activation in the anterior temporal lobe, and because it highlights the impact of specificity of semantic processing.
57. Crinion, J. T., Lambon-Ralph, M. A., Warburton, E. A., Howard, D. & Wise, R. J. S. Temporal lobe regions engaged in normal speech comprehension. Brain 126, 1193-1201 (2003).
58. Scott, S. K., Blank, C. C., Rosen, S. & Wise, R. J. S. Identification of a pathway for intelligible speech in the left temporal lobe. Brain 123, 2400-2406 (2000).
59. Lindenberg, R. & Scheef, L. Supramodal language comprehension: role of the left temporal lobe for listening and reading. Neuropsychologia 45, 2407-2415 (2007).
60. Marinkovic K. et al. Spatiotemporal dynamics of modality-specific and supramodal word processing. Neuron 28, 487-497 (2003). This paper demonstrated the potential of MEG to map the early temporal sequence of regional activation in a semantic paradigm. Auditory and visual stimuli each initially engaged their respective sensory cortices but ultimately the activation from each converged on the anterior temporal lobes.
61. Grabowski, T. J. et al. A role for left temporal pole in the retrieval of words for unique entities. Hum. Brain Mapp. 13, 199-212 (2001).
62. Gorno-Tempini, M. L. & Price, C. J. Identification of famous faces and buildings: a functional neuroimaging study of semantically unique items. Brain 124, 2087-2097 (2001).
63. Nakamura, K. et al. Functional delineation of the human occipito-temporal areas related to face and scene processing: a PET study. Brain 123, 1903-1912 (2000).
64. Gorno-Tempini, M. L. et al. The neural systems sustaining face and proper-name processing. Brain 121, 2103-2118 (1998).
65. Tsukiura, T., Mochizuki-Kawai, H. & Fujii, T. Dissociable roles of the bilateral anterior temporal lobe in face-name associations: an event-related fMRI study. Neuroimage 30, 617-626 (2006).
66. Nakamura, K., et al. Neural substrates for recognition for familiar voices: a PET study. Neuropsychologia 39, 1047-1054 (2001).
67. Snowden, J. S., Thompson, J. C. & Neary D. Knowledge of famous faces and names in semantic dementia. Brain 4, 860-872 (2004).
68. Hodges, J. R., Graham, N. & Patterson, K. Charting the progression in semantic dementia: implications for the organisation of semantic memory. Memory 3, 463-495 (1995).
69. Hodges, J. R., Patterson, K. & Tyler, L. K. Loss of semantic memory: implications for the modularity of mind. Cogn. Neuropsychol. 11, 505-542 (1994).
70. Rogers, T. T., Lambon Ralph, M. A., Hodges, J. R. & Patterson, K. Natural selection: the impact of semantic impairment on lexical and object decision. Cogn. Neuropsychol. 21, 331-352 (2004).
71. Patterson, K. & Erzinçlioglu, S. in Drawing and Non-Verbal Intelligence (eds Lange-Kuettner, C. & Vinter, A.) (Cambridge Univ. Press, Cambridge, in the press).
72. Rogers, T. T. & Patterson, K. Object categorization: reversals and explanations of the basic-level advantage. J. Exp. Psychol. Gen., 136, 451-469 (2007).
73. Gorno-Tempini, M. L., Cipolotti, L. & Price, C. J. Category differences in brain activation studies: where do they come from? Proc. Biol. Sci. 267, 1253-1258 (2000).
74. Gauthier, I., Anderson, A. W., Tarr, M. J., Skudlarski, P. & Gore, J. C. Levels of categorization in visual recognition studied using functional magnetic resonance imaging. Curr. Biol. 7, 645-651 (1997).
75. Tyler, L. K. et al. Processing objects at different levels of specificity. J. Cogn. Neurosci. 16, 351-362 (2004).
76. Buxbaum, L. J. & Saffran, E. M. Knowledge of object manipulation and object function: dissociations in apraxic and nonapraxic subjects. Brain Lang. 82, 179-199 (2002).
77. Chao, L. L. & Martin, A. Representation of manipulable man-made objects in the dorsal stream. Neuroimage 12, 478-484 (2000).
78. Hodges, J. R., Bozeat, S., Lambon Ralph, M. A., Patterson, K. & Spatt, J. The role of conceptual knowledge in object use: evidence from semantic dementia. Brain 123, 1913-1925 (2000).
79. Bozeat, S., Lambon Ralph, M. A., Patterson, K. & Hodges, J. R. When objects lose their meaning: what happens to their use? Cogn. Affect. Behav. Neurosci. 2, 236-251 (2002).
80. Adlam, A. L. et al. Semantic dementia and fluent primary progressive aphasia: two sides of the same coin? Brain 129, 3066-80 (2006).
81. Rogers, T. T., Patterson, K. & Graham, K. S. Colour knowledge in semantic dementia: it's not all black and white. Neuropsychologia (in the press).
82. Rogers, T. T. & McClelland, J. L. Semantic Cognition: A Parallel Distributed Processing Approach (MIT press, Cambridge, Massachusetts, USA, 2004). The general theory of human semantic abilities described in this book explains how we come to know which properties are important for representing which concepts, and why this ability may critically depend upon neuroanatomical convergence within the cortical semantic network.
83. Plaut, D. C. Graded modality-specific specialization in semantics: a computational account of optic aphasia. Cogn. Neuropsychol. 19, 603-639 (2002).
84. Macario, J. F. Young children's use of color in classification: foods and canonically colored objects. Cogn. Dev. 6, 17-46 (1991).
85. Gelman, R. & Williams, E. M. in Handbook of Child Psychology, Vol. II: Cognition, Perception and Development (eds Kuhn, D. & Siegler, R.) 575-530 (Wiley, New York, 1998).
86. Keil, F. C. Concepts, Kinds and Cognitive Development (MIT Press, Cambridge, Massachusetts, USA, 1989).
87. Murphy, G. L. & Medin, D. L. The role of theories in conceptual coherence. Psychol. Rev. 92, 289-316 (1985).
88. Rogers, T. T. et al. Structure and deterioration of semantic memory: a neuropsychological and computational investigation. Psychol. Rev. 111, 205-235 (2004). This paper describes a model implementation of the distributed-plus-hub theory and uses the model to explain many different aspects of the semantic impairment observed in semantic dementia.
89. Garrard, P., Lambon Ralph, M. A., Hodges, J. R. & Patterson, K. Prototypicality, distinctiveness and intercorrelation: analyses of the semantic attributes of living and nonliving items. Cogn. Neuropsychol. 18, 125-174 (2001).
90. Patterson, K. The reign of typicality in semantic memory. philos. Trans. R. Soc. Lond. B Biol. Sci. 362, 813-821 (2007).
91. Hodges, J. R., Patterson, K., Oxbury, S. & Funnell, E. Semantic dementia: progressive fluent aphasia with temporal lobe atrophy. Brain 115, 1783-1806 (1992).
92. Patterson, K. et al. 'Pre-semantic' cognition in semantic dementia: six deficits in search of an explanation. J. Cogn. Neurosci. 18, 169-183 (2006). This paper demonstrates that the amodal semantic deficit in semantic dementia produces the same pattern of impaired performance across a range of tasks differing in modality of input and output.
93. Gloor, P. The Temporal Lobe and Limbic System (OUP, New York, 1997).
94. Hickok, G. & Poeppel, D. The cortical organization of speech processing. Nature Rev. Neurosci. 8, 393-402 (2007).
95. Adolphs, R. & Spezio, M. Role of the amygdala in processing social stimuli. Prog. Brain Res. 156, 363-378 (2006).
96. Martin, A. & Chao, L. L. Semantic memory and the brain: structure and processes. Curr. Opin. Neurobiol. 11, 194-201 (2001).
97. Snodgrass, J. G. & Vanderwart, M. A standardized set of 260 pictures: norms for name agreement, image agreement, familiarity and visual complexity. J. Exp. Psychol. 6, 174-215 (1980).
98. Howard, D. & Patterson, K. Pyramids and Palm Trees: A Test of Semantic Access from Pictures and Words. (Thames Valley test Co., Bury St Edmunds, UK, 1992)
99. Binder, J. R. et al. Human temporal lobe activation by speech and nonspeech sounds. Cereb. Cortex 10, 512-528 (2000).
100. Davis, M. H. & Johnsrude, I. S. Hierarchical processing in spoken language comprehension. J. Neurosci. 23, 3423-3431 (2003).
101. Scott, S. K., Rosen, S., Lang, H. & Wise, R. J. Neural correlates of intelligibility in speech investigated with noise vocoded-speech - a positron emission tomography study. J. Acoust. Soc. Am. 120, 1075-1083 (2006).
102. Ferstl, E. C., Rinck, M. & von Cramon, D. Y. Emotional and temporal aspects of situation model processing during text comprehension: an event-related fMRI study. J. Cogn. Neurosci. 17, 724-739 (2005).
103. Noppeney, U., Price, C. J., Duncan, J. S. & Koepp, M. J. Reading skills after left anterior temporal lobe resection: an fMRI study. Brain 128, 1377-1385 (2005).
104. Devlin, J. T. et al. Is there an anatomical basis for category-specificity? Semantic memory studies in PET and fMRI. Neuropsychologia 40, 54-75 (2002).
105. Noppeney, U. & Price, C. J. Retrieval of visual, auditory, and abstract semantics. Neuroimage 15, 917-926 (2002).
106. Papathanassiou, D. et al. A common language network for comprehension and production: a contribution to the definition of language epicentres with PET. Neuroimage 11, 347-357 (2000).
107. Tranel, D., Grabowski, T. J., Lyon, J. & Damasio, H. Naming the same entities from visual or from auditory stimulation engages similar regions of left inferotemporal cortices. J. Cogn. Neurosci. 17, 1293-1305 (2005).
108. Binder, J. R., Westbury, C. F., McKiernan, K. A., Possing, E. T. & Medler, D. A. Distinct brain systems for processing concrete and abstract concepts. J. Cogn. Neurosci. 17, 905-917(2005).
109. Mummery, C. J., Shallice, T. & Price, C. J. Dual-process model in semantic priming: a functional imaging perspective. Neuroimage 9, 516-525 (1999).
110. Small, D. M., Jones-Gotman, M., Zatorre, R. J., Petrides, M. & Evans A. C. A role for the right anterior temporal lobe in taste quality recognition. J. Neurosci. 17, 5136-5142 (1997).
111. Simons, J. S., Koutstaal, W., Prince, S., Wagner, A. & Schacter, D. Neural mechanisms of visual object priming: evidence for perceptual and semantic distinctions in fusiform cortex. Neuroimage 19, 613-626 (2003).
112. Vuilleumier, P., Henson, R. N., Driver, J. & Dolan, R. J. Multiple levels of visual object constancy revealed by event-related fMRI of repetition priming. Nature Neurosci. 5, 491-499 (2002).
113. Phillips, J. A., Humphreys, G. W., Noppeney, U. & Price, C. J. The neural substrates of action retrieval: an examination of semantic and visual routes to action. Vis. Cogn. 9, 662-684 (2002).
114. Brett, M. The MNI brain and the Talairach atlas. MRC Cognition and Brain Sciences Unit [online] http://imaging.mrc-cbu.cam.ac.uk/imaging/ MniTalairach (2002).